Genetic and molecular mechanisms of aluminum tolerance in plants
C.C. Simões1*, J.O. Melo1*, J.V. Magalhaes2 and C.T. Guimarães2
1Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brasil
2Núcleo de Biologia Aplicada, Embrapa Milho e Sorgo, Sete Lagoas, MG, Brasil
*These authors contributed equally to this study.
Corresponding author: C.T. Guimarães E-mail: claudia@cnpms.embrapa.br
Genet. Mol. Res. 11 (3): 1949-1957 (2012) Received May 29, 2012
Accepted June 25, 2012 Published July 19, 2012
DOI http://dx.doi.org/10.4238/2012.July.19.14
ABSTRACT. Aluminum (Al) toxicity restricts root growth and agricultural yield in acid soils, which constitute approximately 40%
of the potentially arable lands worldwide. The two main mechanisms of Al tolerance in plants are internal detoxification of Al and its exclusion from root cells. Genes encoding membrane transporters and accessory transcription factors, as well as cis-elements that enhance gene expression, are involved in Al tolerance in plants; thus studies of these genes and accessory factors should be the focus of molecular breeding efforts aimed at improving Al tolerance in crops. In this review, we describe the main genetic and molecular studies that led to the identification and cloning of genes associated with Al tolerance in plants. We include recent findings on the regulation of genes associated with Al tolerance. Understanding the genetic, molecular, and physiological aspects of Al tolerance in plants is important for
generating cultivars adapted to acid soils, thereby contributing to food security worldwide.
Key words: Aluminum; Tolerance; Organic acids; Regulatory factors;
QTL INTRODUCTION
Aluminum (Al) toxicity in acid soils is an important abiotic stress factor that reduces crop yield (Ma et al., 2001). In addition to the extensive distribution of acid soils in tropical and subtropical regions, especially in regions where food supply is more tenuous, agricultural activities can also lead to soil acidification (Ciotta et al., 2002). Under acidic conditions, Al is released from soil minerals in ionic forms such as Al(OH)2+, Al(OH)2+, and Al(H2O)63+, with the last species being commonly known as Al3+ (Kinraide et al., 1992). Soil with low pH al- lows for the solubilization and release of Al3+ ions into the rhizosphere, causing a highly toxic effect on sensitive plants (Delhaize and Ryan, 1995).
The effect of Al on plant metabolic processes can be observed within minutes after the onset of the stress syndrome, and is followed by secondary effects that occur at later stages (Kochian, 1995). In the cell wall, Al may bind to carboxyl and phosphate groups due to its high affinity for electron donors such as oxygen (Dale and Sutcliffe, 1986), causing struc- tural changes and compromising cell wall expansion (Ma et al., 2004a). Therefore, Al toxicity causes severe damage to root systems, which consequently reduces water and mineral nutrient uptake, thus limiting agricultural yield (Ma et al., 2001; Kochian et al., 2004).
MECHANISMS OF ALUMINUM TOLERANCE
Mechanisms of Al tolerance are classified as those that prevent Al ions from entering the root apical cells (i.e., apoplastic mechanisms) or that detoxify internal Al (i.e., symplastic mechanisms) (Kochian, 1995; Kochian et al., 2004). In symplastic mechanisms, Al enters the cytoplasm and is detoxified once inside the cell by complexation with organic compounds (Kochian, 1995). Several compounds can form stable complexes with Al inside the cell, in- cluding organic acids such as citrate, oxalate, malate (Foy, 1988; Taylor, 1988; Ma and Miya- saka, 1998), and proteins (Suhayda and Haug, 1985). Free Al3+ or Al complexes with chelating agents can be transported to cell vacuoles, where they are stored without causing toxicity (Kochian et al., 2004).
Apoplastic mechanisms are also known as Al exclusion mechanisms. The following Al exclusion mechanisms have been reported: release of phenolic compounds (Ofei-Manu et al., 2001), mucilage formation (Miyasaka and Hawes, 2001), “pH barrier” resulting from in- creased pH in the rhizosphere (Degenhardt et al., 1998), and organic acid exudation (Delhaize et al., 1993; Pellet et al., 1995; Sasaki et al., 2004; Magalhaes et al., 2007). Roots of several plant species secrete organic acids in response to Al, which are mediated by membrane trans- porters, resulting in the formation of non-toxic complexes with the metal. Thus, this mecha- nism prevents Al from crossing the plasma membrane into the symplast.
Although organic acid exudation is a conserved Al tolerance mechanism being present in different plant species, there are species-specific peculiarities worth noting. The Al-activated
mechanism of malate exudation is well described in wheat (Delhaize et al., 1993; Sasaki et al., 2004), Arabidopsis (Hoekenga et al., 2006), Brassica napus (Ligaba et al., 2006), and rye (Collins et al., 2008), whereas the mechanism of Al tolerance in maize, soybean, sorghum, and barley involves mainly citrate release (Pellet et al., 1995; Yang et al., 2000; Magalhaes et al., 2007; Furukawa et al., 2007; Maron et al., 2010).
Nevertheless, co-occurrence of different Al tolerance mechanisms has been reported in some species. In maize, root citrate (Piñeros et al., 2002) and oxalate (Kidd et al., 2001) exudation are likely involved in Al tolerance. However, Piñeros et al. (2005) observed a low correlation between citrate exudation and Al tolerance in maize, suggesting that this species has other complementary mechanisms enabling them to tolerate Al. In addition to malate, citrate exudation has also been reported to contribute to Al tolerance in wheat, Arabidopsis, and rye (Ryan et al., 2009; Liu et al., 2009; Yokosho et al., 2010). In rice, citrate exudation (Yokosho et al., 2011) as well as symplastic mechanisms are likely to contribute to the extreme Al tolerance in this species (Huang et al., 2009).
ALUMINUM TOLERANCE GENES The ALMT family
The genetic control of the Al tolerance mechanism based on malate exudation is due to the action of genes encoding aluminum-activated malate transporters in the ALMT family.
The first Al tolerance gene to be cloned in plants was designated TaALMT1, which encodes a transporter protein involved in malate exudation from root apices and is responsible for Al tolerance in wheat (Sasaki et al., 2004). TaALMT1 was mapped to chromosome 4DL, co-seg- regating with a major Al tolerance QTL identified in different wheat populations (Raman et al., 2005; Ma et al., 2005). Based on its location, TaALMT1 possibly corresponds to the previously mapped Al tolerance loci, Alt2 (Luo and Dvorák, 1996) and AltBH (Ried and Anderson, 1996).
A large number of ALMT members were implicated in malate exudation and Al toler- ance in Arabidopsis (AtALMT1; Hoekenga et al., 2006), rapeseed (BnALMT1 and BnALMT2;
Ligaba et al., 2006), rye (ScALMT1; Collins et al., 2008), and barley (HvALMT1; Gruber et al., 2010). In contrast, ZmALMT1 (Piñeros et al., 2008) and ZmALMT2 (Ligaba et al., 2012), two members in the ALMT family, were not found to be associated with maize Al tolerance.
The MATE family
Members of the multidrug and toxic compound extrusion (MATE) family have been associated with several cellular processes, including Al tolerance. Al tolerance in sorghum relies mostly on the AltSB locus, which has a major phenotypic effect and has been mapped to sorghum chromosome 3 (Magalhaes et al., 2004). The SbMATE gene mediates Al-activated citrate exudation from root apices and underlies the Al tolerant locus, AltSB (Magalhaes et al., 2007). SbMATE expression is induced with time of exposure to Al and is higher in the root apex compared to the rest of the root (Magalhaes et al., 2007). As in sorghum, Al toler- ance in barley is related to citrate efflux mediated by HvAACT1, which also belongs to the MATE family and is highly expressed in roots of Al-tolerant barley genotypes (Furukawa et al., 2007). QTL mapping in this species has shown that HvAACT1 is located on chromosome
4H, co-localizing with a major QTL that explains more than 50% of the phenotypic variation in Al-activated citrate exudation (Ma et al., 2004b).
Functional MATE homologs associated with Al tolerance were also identified in Ara- bidopsis (AtMATE; Liu et al., 2009), wheat (TaMATE1; Ryan et al., 2009), rye (ScFRDL2;
Yokosho et al., 2010), and rice (OsFRDL4; Yokosho et al., 2011). Some of these genes are located near Al tolerance QTL, such as OsFRDL4, which co-localizes with a QTL on chro- mosome 1 that was detected in different studies (Yokosho et al., 2011). A major Al tolerance QTL explaining 49% of the phenotypic variation was mapped to wheat chromosome 3BL (Navakode et al., 2009), which possibly harbors TaMATE1. According to the authors, this is supported by the fact that this region in wheat is synthenic to sorghum chromosome 3 and rice chromosome 1, where Al tolerance MATE members were located (Navakode et al., 2009).
Two maize MATEs, ZmMATE1 and ZmMATE2, were co-localized with two major Al tolerance QTL on maize chromosomes 6 and 5, respectively (Maron et al., 2010). ZmMATE1 encodes a transmembrane protein that is highly similar to SbMATE, and its overexpression in Arabidopsis results in increased citrate exudation as well as higher Al tolerance (Maron et al., 2010). Al tolerance QTL were mapped to this genomic region of chromosome 6 in two other studies using different mapping populations (Sibov et al., 1999; Ninamango-Cárdenas et al., 2003). In contrast, ZmMATE2 expression, which was not induced by Al, was similar between Al-tolerant and Al-sensitive genotypes (Maron et al., 2010). In addition, association between ZmMATE2 and citrate exudation has not been found, raising questions to a possible role for ZmMATE2 in maize Al tolerance.
ATP-binding cassette (ABC) transporter family
In addition to genes encoding organic acid transporters, other genes have been as- sociated with Al tolerance in plants. Two genes encoding ABC transporters, ALS3 and ALS1, were associated with Al tolerance in Arabidopsis (Larsen et al., 2005, 2007). ALS1 is pri- marily expressed in the root apex and vascular tissues, and ALS1 is present in vacuolar membranes (Larsen et al., 2007). ALS3 is expressed in different organs but mainly in leaf hydathodes and phloem, whereas ALS3 is localized to the plasma membrane (Larsen et al., 2005). Knockout mutants of both genes caused Al hypersensitivity but their overexpression in Arabidopsis did not improve Al tolerance. ALS1 and ALS3 have been hypothesized to act in the intracellular redistribution of Al, keeping this metal away from sensitive tissues (Larsen et al., 2005, 2007).
In rice, sensitive to aluminum rhizotoxicity genes 1 and 2 (STAR1 and STAR2) were identified and the fact that knocking out either star1 or star2 resulted in Al hypersensitivity suggested their function in Al tolerance (Huang et al., 2009). STAR1 encodes a nucleotide- binding domain, whereas STAR2 encodes a transmembrane domain of a bacterial-type ABC transporter, which is involved in UDP-glucose transport (Huang et al., 2009). STAR1 and STAR2 are primarily expressed in the roots and specifically induced by Al, and the proteins en- coded by these genes form a complex that localizes to cytosolic vesicle membranes. Although the mechanism triggered by this transporter is not yet completely understood, the authors sug- gest that UDP-glucose may be involved in cell wall modifications, reducing the toxic effects of Al (Huang et al., 2009). Recently, a half-size ABC transporter encoded by OsALS1 was functionally characterized as responsible for Al sequestration into vacuole, which is required for internal detoxification of this metal in rice (Huang et al., 2012).
Nramp family
Recently, the Nramp aluminum transporter 1 (Nrat1) was found to be associated with Al tolerance in rice. Nrat1 belongs to the natural resistance-associated macrophage protein (Nramp) transporter family (Xia et al., 2010). Nramp proteins are conserved in different species and are involved in divalent ion transport (Courville et al., 2006; Xia et al., 2010). Nrat1 is a transporter located in the plasma membrane of root apical cells, exhibiting transport activity for Al3+, but not for divalent metals or the Al-citrate complex. Nrat1 expression is induced by Al and is root- specific, occurring in all root cells, except for the epidermis. Knockout lines for Nrat1 exhibited higher Al sensitivity, higher Al accumulation in the cell wall, and lower Al concentration in root cells in the presence of Al3+ (Xia et al., 2010). Such findings led the authors to suggest that Nrat1 controls intracellular Al3+ uptake, with subsequent detoxification via transport and Al accumula- tion into cell vacuoles, possibly mediated by OsALS1 (Huang et al., 2012).
REGULATION OF ALUMINUM TOLERANCE GENE EXPRESSION
Due to the close relationship between allelic variation for Al tolerance and the expres- sion of Al tolerance genes, efforts are underway to validate the molecular nature of regula- tory factors involved in Al tolerance. In Arabidopsis, the sensitive to proton rhizotoxicity 1 (STOP1) gene was identified, which encodes a transcription factor involved in Al tolerance (Iuchi et al., 2007; Liu et al., 2009; Sawaki et al., 2009). Initially, Iuchi et al. (2007) described a proton-sensitive Arabidopsis mutant, where a recessive mutation was detected in a gene encoding a Cys2-His2 transcription factor. The stop1 mutant showed reduced root growth un- der low pH conditions and under Al toxicity. Interestingly, these phenotypes were associated with inhibited AtALMT1 gene expression and malate exudation after Al treatment (Iuchi et al., 2007). Microarray analyses of stop1 indicated that multiple genes possibly involved in Al tol- erance are co-regulated by STOP1 (Sawaki et al., 2009). Among those genes is ALS3 (Larsen et al., 2005), which was repressed in the stop1 mutant (Sawaki et al., 2009). Additional studies indicated that STOP1 is also necessary for AtMATE expression and Al-activated citrate exuda- tion in Arabidopsis. Therefore, although both AtALMT1 and AtMATE genes act independently to confer aluminum tolerance in Arabidopsis, the STOP1 transcription factor represents a transcriptional link between them (Liu et al., 2009).
The Al resistance transcription factor 1, ART1, is a rice homologue of AtSTOP1 that regulates the expression of several genes related to rice Al tolerance, such as STAR1 and STAR2 (Yamaji et al., 2009), Nrat1 (Xia et al., 2010), OsFRDL4 (Yokosho et al., 2011) and OsALS1 (Huang et al., 2012).
Cis-elements are located in non-coding regions along the DNA sequence, near or far from the target gene and influence gene expression (von Korff et al., 2009). Cis-acting regula- tory sequences, such as polymorphisms within introns, and modified promoter regions, may influence aluminum tolerance in plants.
In sorghum, the coding region of the aluminum tolerance gene, SbMATE, was identi- cal between Al-tolerant and Al-sensitive genotypes, with polymorphisms being found in the second intron of SbMATE. Furthermore, a tourist-like miniature inverted repeat transposable element (MITE) transposon was detected in the promoter region, and the number of repeats was positively correlated with Al tolerance (Magalhaes et al., 2007). It was then suggested
that the causative mutations underlying aluminum tolerance may have a regulatory nature (Magalhaes et al., 2007).
The TaALMT1 coding region is conserved between Al-tolerant and Al-sensitive lines (Raman et al., 2005). In turn, a 160-bp transposon and eight SNPs were detected downstream of ALMT1, but allelic variation at these loci was not correlated with aluminum tolerance.
However, blocks of tandemly repeated sequences that were duplicated or triplicated were found in genomic regions upstream of the ALMT1 coding region (Sasaki et al., 2006). In general, high ALMT1 gene expression and Al tolerance were correlated with the number of repeats. Subsequently, transgenic plants containing different TaALMT1 promoter alleles were shown to enhance gene expression (Ryan et al., 2010).
An important cis-element for binding the ART1 transcription factor was identified in the STAR1 promoter region, which confers aluminum tolerance in rice (Huang et al., 2009;
Yamaji et al., 2009; Tsutsui et al., 2011). This element consists of the sequence GGN(T/g/a/C) V(C/A/g)S(C/G), located upstream of the STAR1 start codon. Moreover, this element was found in the promoter region of 29 of the 31 genes regulated by ART1 (Yamaji et al., 2009; Tsutsui et al., 2011), including STAR2, Nrat1 (Tsutsui et al., 2011) and OsFRDL4 (Yokosho et al., 2011), which are all involved in rice Al tolerance. In the STAR2 promoter, two copies of this element were identified, in addition to three copies in the Nrat1 (Tsutsui et al., 2011) promoter region.
More recently, a distinct mechanism for regulating HvAACT1 expression was pre- sented in barley (Fujii et al., 2012). An insertion of 1-kb sequence at 6 kb upstream from the HvAACT1 coding region added multiple transcriptional start sites, enhancing this gene expres- sion in the root tips. The modified HvAACT1 expression pattern resulted in a superior Al-in- duced citrate exudation that consequently improved Al tolerance in barley (Fujii et al., 2012).
CONCLUSION
Plants have developed several mechanisms to overcome the limitations imposed by Al toxicity. Despite a prevalence of mechanisms involving organic acid exudation, symplastic mechanisms also play a role in Al tolerance in plants. In some species, Al tolerance is a geneti- cally complex trait, where different tolerance mechanisms coexist. The involvement of multiple mechanisms is apparently independent of the level of tolerance intrinsic to each species, oc- curring in both comparatively Al-sensitive species, such as Arabidopsis, and highly Al-tolerant species, such as rice. Molecular and genetic studies have contributed to the identification of genes associated with Al tolerance. Those genes include membrane transporters of the ALMT, MATE, and ABC families, and functional homologs of these transporter genes are found in dif- ferent species. Transcriptional factors and cis-elements are highly involved in the expression of Al tolerance genes. Integrating information about QTL, genes, and mechanisms involved in Al tolerance allows for a broad understanding of this trait across different plant species. Pyramiding of these genes and tolerance mechanisms by marker-assisted introgression of superior alleles or via genetic transformation may significantly contribute to the development of highly Al tolerant cultivars by molecular breeding, which should contribute to crop production on acid soils.
ACKNOWLEDGMENTS
Research supported by the Minas Gerais Research Foundation (FAPEMIG), the Na-
tional Council for Scientific and Technological Development (CNPq), the Coordination of Improvement of Higher Education Personnel (CAPES), the Generation Challenge Program, McKnight Foundation Collaborative Crop Research Program, and the Brazilian Agricultural Research Corporation (EMBRAPA).
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